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Abstract

Surprising genetic diversity has been discovered in marine holoplankton, organisms that "drift" in water currents throughout their life cycle. This discovery challenges our assumptions and suggests that holoplankton species may have limited dispersal and/or have adapted to small-scale oceanographic features. In this study, I investigated population genetics of <italic>Acartia tonsa</italic>, a holoplanktonic estuarine copepod containing deeply-diverged mitochondrial lineages, on the United States Atlantic coast. The study goals include: 1) assessing its cryptic species/genetic diversity; 2) inferring evolutionary and geographic origins of its cryptic lineages; 3) testing environmental associations of cryptic lineages; 4) inferring evolutionary and ecological processes/mechanisms underlying population diversification of <italic>A. tonsa</italic>.
Phylogenetic analyses of DNA sequences from two gene loci, mitochondrial cytochrome <italic>c</italic> oxidase subunit I (mtCOI) and nuclear ribosomal internal transcribed spacer (nITS), resolved five morphologically cryptic, genetically diverged lineages that were reproductively isolated species based on genealogical concordance principle. Three co-distributed, deeply-diverged mtCOI lineages (<italic>X</italic>, <italic>S</italic>, <italic>F</italic>) showed significant population differentiation within lineages and contrasting phylogeographic patterns among lineages. Population structures and isolation by distance patterns detected for all lineages suggested that dispersal of <italic>Acartia</italic> lineages was more or less limited to adjacent estuaries; geographic isolation was a key mechanism underlying population diversification of <italic>A. tonsa</italic>. The highly diversified, relatively recent lineage <italic>F</italic> demonstrated a southern center of origin in Florida with northward stepwise diversification. Its distinct localized population structure and strong association with low-salinity environments suggested that environmental stressors (such as salinity) could act as physiological barriers to gene flow, facilitating diversification of <italic>Acartia</italic> populations.
Co-existing <italic>Acartia</italic> lineages were parapatrically distributed along the estuarine gradient across systems on the US Atlantic coast. Genetic, morphological and ecological evidence indicated niche partitioning and ecological differentiation of <italic>A. tonsa</italic> within estuaries. Multiple factors may have contributed to the observed parapatric distribution and niche partitioning, including selection by salinity, biological competition, and/or local adaptation. These findings in one of the best known estuarine copepods reinforce the general conclusion that marine biodiversity is substantially underestimated, not only in terms of species numbers, but also with respect to niche partitioning and the potential importance of ecological divergence in marine holoplankton.